Eusocial insect colonies have often been imagined as “superorganisms” exhibiting tight homeostasis at the colony level. However, colonies lack the tight spatial and organizational integration that many multicellular, unitary organisms exhibit. Precise regulation requires rapid feedback, which is often not possible when nestmates are distributed across space, making decisions asynchronously. Thus, one should expect poorer regulation in superorganisms than unitary organisms.Here, I investigate aspects of regulation in collective foraging behaviors that involve both slow and rapid feedback processes. In Chapter 2, I examine a tightly coupled system with near-instantaneous signaling: teams of weaver ants cooperating to transport massive prey items back to their nest. I discover that over an extreme range of scenarios—even up vertical surfaces—the efficiency per transporter remains constant. My results suggest that weaver ant colonies are maximizing their total intake rate by regulating the allocation of transporters among loads. This is an exception that “proves the rule;” the ant teams are recapitulating the physical integration of unitary organisms. Next, I focus on a process with greater informational constraints, with loose temporal and spatial integration. In Chapter 3, I measure the ability of solitarily foraging Ectatomma ruidum colonies to balance their collection of protein and carbohydrates given different nutritional environments. Previous research has found that ant species can precisely collect a near-constant ratio between these two macronutrients, but I discover these studies were using flawed statistical approaches. By developing a quantitative measure of regulatory effect size, I show that colonies of E. ruidum are relatively insensitive to small differences in food source nutritional content, contrary to previously published claims. In Chapter 4, I design an automated, micro-RFID ant tracking system to investigate how the foraging behavior of individuals integrates into colony-level nutrient collection. I discover that spatial fidelity to food resources, not individual specialization on particular nutrient types, best predicts individual forager behavior. These findings contradict previously published experiments that did not use rigorous quantitative measures of specialization and confounded the effects of task type and resource location.

Social insects collectively exploit food sources by recruiting nestmates, creating positive feedback that steers foraging effort to the best locations. The nature of this positive feedback varies among species, with implications for collective foraging. The mass recruitment trails of many ants are nonlinear, meaning that small increases in recruitment effort yield disproportionately large increases in recruitment success. The waggle dance of honeybees, in contrast, is believed to be linear, meaning that success increases proportionately to effort. However, the implications of this presumed linearityhave never been tested. One such implication is the prediction that linear recruiters will equally exploit two identical food sources, in contrast to nonlinear recruiters, who randomly choose only one of them. I tested this prediction in colonies of honeybees that were isolated in flight cages and presented with two identical sucrose feeders. The results from 15 trials were consistent with linearity, with many cases of equal exploitation of the feeders. In addition, I tested the prediction that linear recruiters can reallocate their forager distribution when unequal feeders are swapped in position. Results from 15 trials were consistent with linearity, with many cases of clear choice for a stronger food source, followed by a subsequent switch with reallocation of foragers to the new location of the stronger food source. These findings show evidence of a linear pattern of nestmate recruitment, with implications for how colonies effectively distribute their foragers across available resources.

In many social groups, reproduction is shared between group members, whocompete for position in the social hierarchy for reproductive dominance. This reproductive conflict can lead to different means of enforcing reproductive differences, such as dominance displays or limited control of social hierarchy through antagonistic encounters. In eusocial insects, archetypal colonies contain a single, singly-mated fertile queen, such that no reproductive conflict exists within a colony. However, many eusocial insects deviate from this archetype and have multiply-mated queens (polyandry), multiple queens in a single colony (polygyny), or both. In these cases, reproductive conflict exists between the matrilines and patrilines represented in a colony, specifically over the production of sexual offspring. A possible outcome of reproductive conflict may be the emergence of cheating lineages, which favor the production of sexual offspring, taking advantage of the worker force produced by nestmate queens and/or patrilines. In extreme examples, inquiline social parasites may be an evolutionary consequence of reproductive conflict between nestmate queens. Inquiline social parasitism is a type of social parasitism that is usually defined by a partial or total loss of the worker caste, and the “infiltration” of host colonies to take advantage of the host worker force for reproduction. It has been hypothesized that these inquiline social parasites evolve through the speciation of cheating queen lineages from within their incipient host species. This “intra- specific” origin model involves a foundational hypothesis that the common ancestor of host and parasite (and thus, putatively, the host at the time of speciation) should be functionally polygynous, and that parasitism evolves as a “resolution” of reproductive conflict in colonies. In this dissertation, I investigate the hypothesized role of polygyny in the evolution of inquiline social parasites. I use molecular ecology and statistical approaches to validate the role of polygyny in the evolution of some inquiline social parasites. I further discuss potential mechanisms for the evolution and speciation of social parasites, and discuss future directions to elucidate these mechanisms.

The flexibility and robustness of social insect colonies, when they cope with challenges as integrated units, raise many questions, such as how hundreds and thousands of individual local responses are coordinated without a central controlling process. Answering such questions requires: 1. Quantifiable collective responses of colonies under specific scenarios; 2. Decomposability of the collective colony-level response into individual responses; and 3. Mechanisms to integrate the colony- and individual-level responses. In the first part of my dissertation, I explore coordinated collective responses of colonies in during the alarm response to an alarmed nestmate (chapter 2&3). I develop a machine-learning approach to quantitatively estimate the collective and individual alarm response (chapter 2). Using this methodology, I demonstrate that colony alarm responses to the introduction of alarmed nestmates can be decomposed into immediately cascading, followed by variable dampening processes. Each of those processes are found to be modulated by variation in individual alarm responsiveness, as measured by alarm response threshold and persistence of alarm behavior. This variation is modulated in turn by environmental context, in particular with task-related social context (chapter 3). In the second part of my dissertation, I examine the mechanisms responsible for colonial changes in metabolic rate during ontogeny. Prior studies have found that larger ant colonies (as for larger organisms) have lower mass-specific metabolic rates, but the mechanisms remain unclear. In a 3.5-year study on 25 colonies, metabolic rates of colonies and colony components were measured during ontogeny (chapter 4). The scaling of metabolic rate during ontogeny was fit better by segmented regression or quadratic regression models than simple linear regression models, showing that colonies do not follow a universal power-law of metabolism during the ontogenetic development. Furthermore, I showed that the scaling of colonial metabolic rates can be primarily explained by changes in the ratio of brood to adult workers, which nonlinearly affects colonial metabolic rates. At high ratios of brood to workers, colony metabolic rates are low because the metabolic rate of larvae and pupae are much lower than adult workers. However, the high colony metabolic rates were observed in colonies with moderate brood: adult ratios, because higher ratios cause adult workers to be more active and have higher metabolic rates, presumably due to the extra work required to feed more brood.

An insect society needs to share information about important resources in order to collectively exploit them. This task poses a dilemma if the colony must consider multiple resource types, such as food and nest sites. How does it allocate workers appropriately to each resource, and how does it adapt its recruitment communication to the specific needs of each resource type? In this dissertation, I investigate these questions in the ant Temnothorax rugatulus.

In Chapter 1, I summarize relevant past work on food and nest recruitment. Then I describe T. rugatulus and its recruitment behavior, tandem running, and I explain its suitability for these questions. In Chapter 2, I investigate whether food and nest recruiters behave differently. I report two novel behaviors used by recruiters during their interaction with nestmates. Food recruiters perform these behaviors more often than nest recruiters, suggesting that they convey information about target type. In Chapter 3, I investigate whether colonies respond to a tradeoff between foraging and emigration by allocating their workforce adaptively. I describe how colonies responded when I posed a tradeoff by manipulating colony need for food and shelter and presenting both resources simultaneously. Recruitment and visitation to each target partially matched the predictions of the tradeoff hypothesis. In Chapter 4, I address the tuned error hypothesis, which states that the error rate in recruitment is adaptively tuned to the patch area of the target. Food tandem leaders lost followers at a higher rate than nest tandem leaders. This supports the tuned error hypothesis, because food targets generally have larger patch areas than nest targets with small entrances.

This work shows that animal groups face tradeoffs as individual animals do. It also suggests that colonies spatially allocate their workforce according to resource type. Investigating recruitment for multiple resource types gives a better understanding of exploitation of each resource type, how colonies make collective decisions under conflicting goals, as well as how colonies manage the exploitation of multiple types of resources differently. This has implications for managing the health of economically important social insects such as honeybees or invasive fire ants.

Animals have evolved a diversity of signaling traits, and in some species, they co-occur and are used simultaneously to communicate. Although much work has been done to understand why animals possess multiple signals, studies do not typically address the role of inter-signal interactions, which may vary intra- and inter-specifically and help drive the evolutionary diversity in signals. For my dissertation, I tested how angle-dependent structural coloration, courtship displays, and the display environment interact and co-evolved in hummingbird species from the “bee” tribe (Mellisugini). Most “bee” hummingbird species possess an angle-dependent structurally colored throat patch and stereotyped courtship (shuttle) display. For 6 U.S. “bee” hummingbird species, I filmed male shuttle displays and mapped out the orientation- and-position-specific movements during the displays. With such display paths, I was able to then recreate each shuttle display in the field by moving plucked feathers from each male in space and time, as if they were naturally displaying, in order to measure each male’s color appearance during their display (i.e. the interactions between male hummingbird plumage, shuttle displays, and environment) from full-spectrum photographs. I tested how these interactions varied intra- and inter-specifically, and which of these originating traits might explain that variation. I first found that the solar-positional environment played a significant role in explaining variation in male color appearance within two species (Selasphorus platycercus and Calypte costae), and that different combinations of color-behavior-environment interactions made some males (in both species) appear bright, colorful, and flashy (i.e. their color appearance changes throughout a display), while other males maintained a consistent (non-flashing) color display. Among species, I found that plumage flashiness positively co-varied with male display behaviors, while another measure of male color appearance (average brightness/colorfulness) co-varied with the feather reflectance characteristics themselves. Additionally, species that had more exaggerated plumage features had less exaggerated shuttle displays. Altogether, my dissertation work illustrates the complexity of multiple signal evolution and how color-behavior-environment interactions are vital to understanding the evolution of colorful and behavioral display traits in animals.

For interspecific mutualisms, the behavior of one partner can influence the fitness of the other, especially in the case of symbiotic mutualisms where partners live in close physical association for much of their lives. Behavioral effects on fitness may be particularly important if either species in these long-term relationships displays personality. Animal personality is defined as repeatable individual differences in behavior, and how correlations among these consistent traits are structured is termed behavioral syndromes. Animal personality has been broadly documented across the animal kingdom but is poorly understood in the context of mutualisms. My dissertation focuses on the structure, causes, and consequences of collective personality in Azteca constructor colonies that live in Cecropia trees, one of the most successful and prominent mutualisms of the neotropics. These pioneer plants provide hollow internodes for nesting and nutrient-rich food bodies; in return, the ants provide protection from herbivores and encroaching vines. I first explored the structure of the behavioral syndrome by testing the consistency and correlation of colony-level behavioral traits under natural conditions in the field. Traits were both consistent within colonies and correlated among colonies revealing a behavioral syndrome along a docile-aggressive axis. Host plants of more active, aggressive colonies had less leaf damage, suggesting a link between a colony personality and host plant health. I then studied how aspects of colony sociometry are intertwined with their host plants by assessing the relationship among plant growth, colony growth, colony structure, ant morphology, and colony personality. Colony personality was independent of host plant measures like tree size, age, volume. Finally, I tested how colony personality influenced by soil nutrients by assessing personality in the field and transferring colonies to plants the greenhouse under different soil nutrient treatments. Personality was correlated with soil nutrients in the field but was not influenced by soil nutrient treatment in the greenhouse. This suggests that soil nutrients interact with other factors in the environment to structure personality. This dissertation demonstrates that colony personality is an ecologically relevant phenomenon and an important consideration for mutualism dynamics.

The coordination of group behavior in the social insects is representative of a broader phenomenon in nature, emergent biological complexity. In such systems, it is believed that large-scale patterns result from the interaction of relatively simple subunits. This dissertation involved the study of one such system: the social foraging of the ant Temnothorax rugatulus. Physically tiny with small population sizes, these cavity-dwelling ants provide a good model system to explore the mechanisms and ultimate origins of collective behavior in insect societies. My studies showed that colonies robustly exploit sugar water. Given a choice between feeders unequal in quality, colonies allocate more foragers to the better feeder. If the feeders change in quality, colonies are able to reallocate their foragers to the new location of the better feeder. These qualities of flexibility and allocation could be explained by the nature of positive feedback (tandem run recruitment) that these ants use. By observing foraging colonies with paint-marked ants, I was able to determine the `rules' that individuals follow: foragers recruit more and give up less when they find a better food source. By altering the nutritional condition of colonies, I found that these rules are flexible - attuned to the colony state. In starved colonies, individual ants are more likely to explore and recruit to food sources than in well-fed colonies. Similar to honeybees, Temmnothorax foragers appear to modulate their exploitation and recruitment behavior in response to environmental and social cues. Finally, I explored the influence of ecology (resource distribution) on the foraging success of colonies. Larger colonies showed increased consistency and a greater rate of harvest than smaller colonies, but this advantage was mediated by the distribution of resources. While patchy or rare food sources exaggerated the relative success of large colonies, regularly (or easily found) distributions leveled the playing field for smaller colonies. Social foraging in ant societies can best be understood when we view the colony as a single organism and the phenotype - group size, communication, and individual behavior - as integrated components of a homeostatic unit.

For over a century, researchers have been investigating collective cognition, in which a group of individuals together process information and act as a single cognitive unit. However, I still know little about circumstances under which groups achieve better (or worse) decisions than individuals. My dissertation research directly addressed this longstanding question, using the house-hunting ant Temnothorax rugatulus as a model system. Here I applied concepts and methods developed in psychology not only to individuals but also to colonies in order to investigate differences of their cognitive abilities. This approach is inspired by the superorganism concept, which sees a tightly integrated insect society as the analog of a single organism. I combined experimental manipulations and models to elucidate the emergent processes of collective cognition. My studies show that groups can achieve superior cognition by sharing the burden of option assessment among members and by integrating information from members using positive feedback. However, the same positive feedback can lock the group into a suboptimal choice in certain circumstances. Although ants are obligately social, my results show that they can be isolated and individually tested on cognitive tasks. In the future, this novel approach will help the field of animal behavior move towards better understanding of collective cognition.